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Trends in Ranavirus Prevalence Among Plethodontid Salamanders in the Great Smoky Mountains National Park

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Abstract

Emerging pathogens are a potential contributor to global amphibian declines. Ranaviruses, which infect ectothermic vertebrates and are common in aquatic environments, have been implicated in die-offs of at least 72 amphibian species worldwide. Most studies on the subject have focused on pool-breeding amphibians, and infection trends in other amphibian species assemblages have been understudied. Our primary study objective was to evaluate hypotheses explaining ranavirus prevalence within a lungless salamander assemblage (Family Plethodontidae) in the Great Smoky Mountains National Park, USA. We sampled 566 total plethodontid salamanders representing 14 species at five sites over a 6-year period (2007–2012). We identified ranavirus-positive individuals in 11 of the 14 (78.6%) sampled species, with salamanders in the genus Desmognathus having greatest infection prevalence. Overall, we found the greatest support for site elevation and sampling year determining infection prevalence. We detected the greatest number of infections in 2007 with 82.5% of sampled individuals testing positive for ranavirus, which we attribute to record drought during this year. Infection prevalence remained relatively high in low-elevation sites in 2008 and 2009. Neither body condition nor aquatic dependence was a significant predictor of ranavirus prevalence. Overall, our results indicate that life history differences among species play a minor role determining ranavirus prevalence compared to the larger effects of site elevation and yearly fluctuations (likely due to environmental stressors) during sampling years.

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References

  • Acevedo-Whitehouse K, Duffus ALJ (2009) Effects of environmental change on wildlife health. Philisophical Transactions of the Royal Society B 364:3429‒3438.

    Article  Google Scholar 

  • Balseiro A, Dalton KP, del Cerro A, Marquez I, Cunningham AA, Parra F, et al. (2009) Pathology, isolation and molecular characterization of a ranavirus from the common midwife toad Alytes obstetricans on the Iberian Peninsula. Diseases of Aquatic Organisms 84:95–104.

    Article  CAS  PubMed  Google Scholar 

  • Barrett, K, Guyer, C (2008) Differential responses of amphibians and reptiles in riparian and stream habitats to land use disturbances in western Georgia, USA. Biol. Conserv. 141:2290–2300.

    Article  Google Scholar 

  • Blaustein AR, Gervasi SS, Johnson PTJ, Hoverman JT, Belden LK, Bradley PW, et al. (2012) Ecophysiology meets conservation: understanding the role of disease in amphibian population declines. Philosophical Transactions of the Royal Society B 367:1688‒1707.

    Article  Google Scholar 

  • Brunner JL, Schock DM, Davdison EW, Collins JP (2004) Intraspecific reservoirs: complex life history and the persistence of a lethal ranavirus. Ecology 85:560–566.

    Article  Google Scholar 

  • Brunner JL, Barnett KE, Gosier CJ, McNulty SA, Rubbo MJ, Kolozsvary MB (2011) Ranavirus infection die-offs of vernal pool amphibians in New York, USA. Herpetological Review 42:76–79.

    Google Scholar 

  • Bryan LK, Baldwin CA, Gray MJ, Miller DL (2009) Efficacy of select disinfectants at inactivating Ranavirus. Diseases of Aquatic Organisms 84:89–94.

    Article  CAS  PubMed  Google Scholar 

  • Byappanahalli M, Fowler M, Shively D, Whitman R (2003) Ubiquity and persistence of Escherichia coli within a midwestern stream. Applied Environmental Microbiology 69:4549‒4555.

    Article  CAS  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information-theoretic approach, 2nd ed., New York: Springer

    Google Scholar 

  • Caruso NM, Lips KR (2013) Truly enigmatic declines in terrestrial salamander populations in Great Smoky Mountains National Park. Diversity and Distributions 19:38–48.

    Article  Google Scholar 

  • Collins JP, Storfer A (2003) Global amphibian declines: sorting the hypotheses. Diversity and Distributions 9:89–98.

    Article  Google Scholar 

  • Corser JD (2001) Decline of disjunct green salamander (Aneides aeneus) populations in the southern Appalachians. Biological Conservation 97:119–126.

    Article  Google Scholar 

  • Crother BI (editor) (2012) Scientific and Standard English Names of Amphibians and Reptiles of North America North of Mexico, with Comments Regarding Confidence in our Understanding, 7th ed., SSAR Circular # 39

  • Davic RD, Welsh HH, Jr (2004) On the ecological roles of salamanders. Annual Review of Ecology and Systematics 35:404–434.

    Google Scholar 

  • Davis AK, DeVore JL, Milanovich JR, Cecala K, Maerz JC, Yabsley MJ (2009) New findings from an old pathogen: intraerythrocytic bacteria (Family Anaplasmatacea) in red-backed salamanders (Plethodon cinereus). Ecohealth 6:219–228.

    Article  PubMed  Google Scholar 

  • Feder ME (1983) Integrating the ecology and physiology of plethodontid salamanders. Herpetologica 39:291‒310.

    Google Scholar 

  • Fox SF, Greer AL, Torres-Cervantes R, Collins JP (2006) First case of ranavirus-associated morbidity and mortality in natural populations of the South American frog Atelognathus patagoncius. Diseases of Aquatic Organisms 72:87–92.

    Article  PubMed  Google Scholar 

  • Geng Y, Wang KY, Zhou ZY, Li CW, Wang J, He M, et al. (2011) First report of a Ranavirus associated with morbidity and mortality in farmed Chinese giant salamanders (Andrias davidianus). Journal of Comparative Pathology 145:95–102.

    Article  CAS  PubMed  Google Scholar 

  • Gray MJ, Miller DL, Hoverman JT (2009a) Ecology and pathology of amphibian ranaviruses. Diseases of Aquatic Organisms 87:243–266.

    Article  PubMed  Google Scholar 

  • Gray MJ, Miller DL, Hoverman JT (2009b) First report of Ranavirus infecting lungless salamanders. Herpetological Review 40:316–319.

    Google Scholar 

  • Gray MJ, Miller DL, Hoverman JT (2012) Reliability of non-lethal surveillance methods for detecting ranavirus infection. Diseases of Aquatic Organisms 99:1–6.

    Article  CAS  PubMed  Google Scholar 

  • Gray MJ, Miller DL (2013) The rise of ranavirus: an emerging pathogen threatens ectothermic vertebrates. Wildlife Professional 7:51-55

    Google Scholar 

  • Greer AL, Briggs CJ, Collins JP (2008) Testing a key assumption of host-pathogen theory: density and disease transmission. Oikos 117:1667–1673.

    Article  Google Scholar 

  • Haislip NA, Gray MJ, Hoverman JT, Miller DL (2011) Development and disease: how susceptibility to an emerging pathogen changes through anuran development. PLoS ONE 6:1–6.

    Article  Google Scholar 

  • Hoverman JT, Gray MJ, Miller DL (2010) Anuran susceptibilities to ranaviruses: role of species identity, exposure route, and a novel virus isolate. Diseases of Aquatic Organisms 89:97–107.

    Article  PubMed  Google Scholar 

  • Hoverman JT, Gray MJ, Haislip NA, Miller DL (2011) Phylogeny, life history, and ecology contribute to differences in anuran susceptibility to ranaviruses. Ecohealth 8:301–319.

    Article  PubMed  Google Scholar 

  • Hoverman JT, Gray MJ, Miller DL, Haislip NA (2012) Widespread occurrence of ranavirus in pond-breeding amphibian populations. Ecohealth 9:36‒48.

    Article  PubMed  Google Scholar 

  • Kiesecker JM, Blaustein AR, Belden LK (2001) Complex causes of amphibian populations declines. Nature 410:681–684.

    Article  CAS  PubMed  Google Scholar 

  • Kroschel WA, Sutton WB, McClure CJW, Pauley TK (2014) Decline of the Cheat Mountain salamander over a 32-year period and the potential influence of competition from a sympatric species. Journal of Herpetology 48:415–422.

    Article  Google Scholar 

  • Kundzewicz ZW, Mata LJ, Arnell NW, Döll P, Jimenez B, Miller K, et al. (2008) The implications of projected climate change for freshwater resources and their management. Hydrological Sciences Journal 53:3–10.

    Article  Google Scholar 

  • Langdon JS (1989) Experimental transmission and pathogenicity of epizootic hematopoietic necrosis virus (EHNV) in redfin perch, Perca fluviatilis L. and 11 other teleosts. Journal of Fish Diseases 12:295–310.

    Article  Google Scholar 

  • Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, Voyles J, et al. (2006) Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the National Academy of Sciences 103:3165–3170.

    Article  CAS  Google Scholar 

  • Martel A, Spitzen-van der Sluijs A, Blooi M., Bert W, Ducatelle R, Fisher MC, et al. (2013) Batrachochytrium salamandrivorans sp. nov. causes lethal chytridomycosis in amphibians. Proceedings of the National Academy of Sciences of the USA 110:15325–15329.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martel A, Blooi M, Adriaensen C, Rooij Van P, Beukema W, Fisher MC, et al. (2014) Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science 31:630–631.

    Article  Google Scholar 

  • Mendelson JR, Lips KR, Gagliardo RW, Rabb GB, Collins JP, Diffendorfer JE, et al. (2006) Confronting amphibian declines and extinctions. Science 313:48.

    Article  CAS  PubMed  Google Scholar 

  • Miller D, Gray M, Storfer A (2011) Ecopathology of ranaviruses infecting amphibians. Viruses 2011:2351–2373.

    Article  Google Scholar 

  • Nazir J, Spengler M, Marschang RE (2012) Environmental persistence of amphibian and reptilian ranaviruses. Diseases of Aquatic Organisms 98:177–184.

    Article  CAS  PubMed  Google Scholar 

  • Petranka JW (1998) Salamanders of the United States and Canada, Washington, DC and London, UK: Smithsonian Institution Press.

    Google Scholar 

  • Petranka JW, Murray SS (2001) Effectiveness of removal sampling for determining salamander density and biomass: a case study in an Appalachian streamside community. Journal of Herpetology 35:36–44.

    Article  Google Scholar 

  • Petranka JW, Murray SS, Kennedy CA (2003) Responses of amphibians to restoration of a southern Appalachian wetland: perturbations confound post-restoration assessment. Wetlands 23:278–290.

    Article  Google Scholar 

  • Petranka JW, Harp EM, Holbrook CT, Hamel JA (2007) Long-term persistence of amphibian populations in a restored wetland complex. Biological Conservation 138:371–380.

    Article  Google Scholar 

  • Picco AM, Brunner JL, Collins JP (2007) Susceptibility of the endangered California tiger salamander, Ambystoma californiense, to ranavirus infection. Journal of Wildlife Diseases 43:286–290.

    Article  PubMed  Google Scholar 

  • R Core Team (2013) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Rothermel BB, Travis ER, Miller DL, Hill RL, McGuire JL, Yabsley MJ (2013) High occupancy of stream salamanders despite high ranavirus prevalence in a southern Appalachians watershed. EcoHealth DOI: 10.1007/s10393-013-0843-5.

    PubMed  Google Scholar 

  • Rovito SM, Parra-Olea G, Vásquez-Almazán CR, Papenfuss TJ, Wake DB (2009) Dramatic declines in Neotropical salamander populations are an important part of the global amphibian crisis. Proceedings of the National Academy of Sciences of the USA 106:3231–3236.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schulte-Hostedde A, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163.

    Article  Google Scholar 

  • Sousa MJ, Gray MJ, Colclough P, Miller DL (2012) Prevalence of infection by Batrachochytrium dendrobatidis and ranavirus in eastern hellbenders (Cryptobranchus alleganiensis alleganiensis) in eastern Tennessee. Journal of Wildlife Diseases 48:560–566.

    Article  Google Scholar 

  • St-Amour V, Garner TWJ, Shulte-Hostedde AI, Lesbarrères D (2010) Effects of two amphibian pathogens on the developmental stability of green frogs. Conservation Biology 24:788–794.

    Article  PubMed  Google Scholar 

  • Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, et al. (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786.

    Article  CAS  PubMed  Google Scholar 

  • Teacher AGF, Cunningham AA, Garner TWJ (2010) Assessing the long-term impact of Ranavirus infection in wild common frog populations. Animal Conservation 13:514–522.

    Article  Google Scholar 

  • Tilley SG, Huheey JE (2001) Reptiles and Amphibians of the Smokies, Gatlinburg, TN: Great Smoky Mountains Natural History Association.

    Google Scholar 

  • Une Y, Sakuma A, Matsueda H, Nakai K, Murakam M (2009) Ranavirus outbreak in North American bullfrogs (Rana catesbeiana), Japan, 2008. Emerging Infectious Diseases 15:1146–1147.

    Article  PubMed Central  PubMed  Google Scholar 

  • Wake DB, Vredenburg VT (2009) Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proceedings of the National Academy of Sciences 105:11466–11473.

    Article  Google Scholar 

  • Wells KD (2007) The Ecology and Behavior of Amphibians, Chicago, IL: The University of Chicago Press.

    Book  Google Scholar 

  • Welsh HH, Jr, Droege S (2001) A case for using plethodontid salamanders for monitoring biodiversity and ecosystem integrity of North American forests. Conservation Biology 15:558–569.

    Article  Google Scholar 

  • Whiles MR, Lips KR, Pringle CM, Kilham SS, Bixby RJ, Brenes R, et al. (2006) The effects of amphibian population declines on the structure and function of Neotropical stream ecosystems. Frontiers in Ecology and the Environment 4:27–34.

    Article  Google Scholar 

  • Whitfield SM, Geerdes E, Chacon I, Ballestero Rodriguez E, Jimenez RR, Donnelly MA, Kerby JL (2013) Infection and co-infection by the amphibian chytrid fungus and ranavirus in wild Costa Rican frogs. Diseases of Aquatic Organisms 104:173–178.

    Article  PubMed  Google Scholar 

  • Whitman RL, Gochee AV, Dustman WA, Kennedy KJ (1995) Use of coliform bacteria in assessing human sewage contamination. Natural Areas Journal 15:227‒233.

    Google Scholar 

  • Wyman RL (1998) Experimental assessment of salamanders as predators of detrital food webs: effects on invertebrates, decomposition and the carbon cycle. Biodiversity and Conservation 7:641–650.

    Article  Google Scholar 

Download references

Acknowledgments

We thank R. Brenes, M. Brand, L. Henderson, along with multiple student volunteers from the University of Tennessee Department of Forestry, Wildlife and Fisheries and Pellissippi State Community College for field sampling assistance; and M. Niemiller and K. Hamed for assistance with salamander identification. Funds for this research were provided by the U.S. National Park Service (GSMNP) and the University of Tennessee Institute of Agriculture. We thank the Barrett lab, H. Rothbone, D. Steen, S. Sterrett, and E. Ridell for comments on earlier versions of this manuscript.

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Correspondence to William B. Sutton.

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Sutton, W.B., Gray, M.J., Hoverman, J.T. et al. Trends in Ranavirus Prevalence Among Plethodontid Salamanders in the Great Smoky Mountains National Park. EcoHealth 12, 320–329 (2015). https://doi.org/10.1007/s10393-014-0994-z

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